Metabolic Brain Disease

, Volume 30, Issue 5, pp 1193–1206 | Cite as

Possible cause for altered spatial cognition of prepubescent rats exposed to chronic radiofrequency electromagnetic radiation

  • Sareesh Naduvil Narayanan
  • Raju Suresh Kumar
  • Kalesh M. Karun
  • Satheesha B. Nayak
  • P. Gopalakrishna Bhat
Research Article

Abstract

The effects of chronic and repeated radiofrequency electromagnetic radiation (RFEMR) exposure on spatial cognition and hippocampal architecture were investigated in prepubescent rats. Four weeks old male Wistar rats were exposed to RF-EMR (900 MHz; SAR-1.15 W/kg with peak power density of 146.60 μW/cm2) for 1 h/day, for 28 days. Followed by this, spatial cognition was evaluated by Morris water maze test. To evaluate the hippocampal morphology; H&E staining, cresyl violet staining, and Golgi-Cox staining were performed on hippocampal sections. CA3 pyramidal neuron morphology and surviving neuron count (in CA3 region) were studied using H&E and cresyl violet stained sections. Dendritic arborization pattern of CA3 pyramidal neuron was investigated by concentric circle method. Progressive learning abilities were found to be decreased in RF-EMR exposed rats. Memory retention test performed 24 h after the last training revealed minor spatial memory deficit in RF-EMR exposed group. However, RF-EMR exposed rats exhibited poor spatial memory retention when tested 48 h after the final trial. Hirano bodies and Granulovacuolar bodies were absent in the CA3 pyramidal neurons of different groups studied. Nevertheless, RF-EMR exposure affected the viable cell count in dorsal hippocampal CA3 region. RF-EMR exposure influenced dendritic arborization pattern of both apical and basal dendritic trees in RF-EMR exposed rats. Structural changes found in the hippocampus of RF-EMR exposed rats could be one of the possible reasons for altered cognition.

Keywords

Mobile phone Cognition Prepubescent rat Hippocampus Morris water maze 

References

  1. Aksoy U, Sahin S, Ozkoc S, Ergor G (2005) The effect of electromagnetic waves on the growth of Entamoeba histolytica and Entamoeba dispar. Saudi Med J 26(9):1388–1390PubMedGoogle Scholar
  2. Alvernhe A, Van Cauter T, Save E, Poucet B (2008) Different CA1 and CA3 representations of novel routes in a shortcut situation. J Neurosci 28(29):7324–7333CrossRefPubMedGoogle Scholar
  3. Avital A, Richter-Levin G (2005) Exposure to juvenile stress exacerbates the behavioural consequences of exposure to stress in the adult rat. Int J Neuropsychopharmacol 8:163–173CrossRefPubMedGoogle Scholar
  4. Bancroft JD, Stevens A (1990) Pigments and minerals. In: Bancroft JD, Stevens A (eds) Theory and practice of histological techniques, 3rd edn. Churchill Livingstone, New York, p 262Google Scholar
  5. Bas O, Odaci E, Kaplan S, Acer N, Ucok K, Colakoglu S (2009) 900 MHz electromagnetic field exposure affects qualitative and quantitative features of hippocampal pyramidal cells in the adult female rat. Brain Res 1265:178–185CrossRefPubMedGoogle Scholar
  6. Beckstead RM (1978) Afferent connections of the entorhinal area in the rat as demonstrated by retrograde cell-labelling with horse-radish peroxidase. Brain Res 152:249–264CrossRefPubMedGoogle Scholar
  7. Bouji M, Lecomte A, Hode Y, de Seze R, Villégier AS (2012) Effects of 900 MHz radiofrequency on corticosterone, emotional memory and neuroinflammation in middle-aged rats. Exp Gerontol 47(6):444–451. doi:10.1016/j.exger.2012.03.015, Epub 2012 Apr 6 CrossRefPubMedGoogle Scholar
  8. Burgess N, Maguire EA, O’Keefe J (2002) The human hippocampus and spatial and episodic memory. Neuron 35(4):625–641CrossRefPubMedGoogle Scholar
  9. Chavdoula ED, Panagopoulos DJ, Margaritis LH (2010) Comparison of biological effects between continuous and intermittent exposure to GSM-900-MHz mobile phone radiation: detection of apoptotic cell-death features. Mutat Res 700(1–2):51–61CrossRefPubMedGoogle Scholar
  10. Chen KH, Reese EA, Kim HW, Rapoport SI, Rao JS (2011) Disturbed neurotransmitter transporter expression in Alzheimer’s disease brain. J Alzheimers Dis 26(4):755–766. doi:10.3233/JAD-2011-110002 PubMedCentralPubMedGoogle Scholar
  11. Dasdag S, Akdag MZ, Ulukaya E, Uzunlar AK, Ocak AR (2009) Effect of mobile phone exposure on apoptotic glial cells and status of oxidative stress in rat brain. Electromagn Biol Med 28(4):342–354CrossRefPubMedGoogle Scholar
  12. Disterhoft JF, Moyer JR Jr, Thompson LT (1994) The calcium rationale in aging and Alzheimer’s disease. Evidence from an animal model of normal aging. Ann N Y Acad Sci 747:382–406CrossRefPubMedGoogle Scholar
  13. Finnie JW, Blumbergs PC, Manavis J, Utteridge TD, Gebski V, Davies RA, Vernon-Roberts B, Kuchel TR (2002) Effect of long-term mobile communication microwave exposure on vascular permeability in mouse brain. Pathology 34(4):344–347CrossRefPubMedGoogle Scholar
  14. Fragopoulou AF, Miltiadous P, Stamatakis A, Stylianopoulou F, Koussoulakos SL, Margaritis LH (2010) Whole body exposure with GSM 900 MHz affects spatial memory in mice. Pathophysiology 17(3):179–187CrossRefPubMedGoogle Scholar
  15. Good M (2002) Spatial memory and Hippocampal function: where are we now? Psicológica 23:109–138Google Scholar
  16. Hao D, Yang L, Chen S, Tong J, Tian Y, Su B, Wu S, Zeng Y (2013) Effects of long-term electromagnetic field exposure on spatial learning and memory in rats. Neurol Sci 34(2):157–164. doi:10.1007/s10072-012-0970-8, Epub 2012 Feb 24 CrossRefPubMedGoogle Scholar
  17. Hosseini-Sharifabad M, Esfandiari E, Hosseini-Sharifabad A (2012) The effect of prenatal exposure to restraint stress on hippocampal granule neurons of adult rat offspring. Iran J Basic Med Sci 15(5):1060–1067PubMedCentralPubMedGoogle Scholar
  18. IARC (International Agency for Research on Cancer) of World Health Organization (2011) “IARC classifies radiofrequency electromagnetic fields as possibly carcinogenic to humans”, press release No 208. http://www.iarc.fr/en/media-centre/pr/2011/pdfs/pr208_E.pdf
  19. Isgor C, Kabbaj M, Akil H, Watson SJ (2004) Delayed effects of chronic variable stress during peripubertal-juvenile period on hippocampal morphology and on cognitive and stress axis functions in rats. Hippocampus 14:636–648CrossRefPubMedGoogle Scholar
  20. Ishida A, Ueda Y, Ishida K, Misumi S, Masuda T, Fujita M, Hida H (2011) Minor neuronal damage and recovered cellular proliferation in the hippocampus after continuous unilateral forelimb restraint in normal rats. J Neurosci Res 89(3):457–465CrossRefPubMedGoogle Scholar
  21. Jiang DP, Li J, Zhang J, Xu SL, Kuang F, Lang HY, Wang YF, An GZ, Li JH, Guo GZ (2013) Electromagnetic pulse exposure induces overexpression of beta amyloid protein in rats. Arch Med Res 44(3):178–184. doi:10.1016/j.arcmed.2013.03.005 CrossRefPubMedGoogle Scholar
  22. Jo YS, Park EH, Kim IH, Park SK, Kim H, Kim HT, Choi JS (2007) The medial prefrontal cortex is involved in spatial memory retrieval under partial-cue conditions. J Neurosci 27(49):13567–13578CrossRefPubMedGoogle Scholar
  23. Jung MW, Wiener SI, McNaughton BL (1994) Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat. J Neurosci 14(12):7347–7356PubMedGoogle Scholar
  24. Kesari KK, Kumar S, Behari J (2011) 900-MHz microwave radiation promotes oxidation in rat brain. Electromagn Biol Med 30(4):219–234. doi:10.3109/15368378.2011.587930 CrossRefPubMedGoogle Scholar
  25. Kesari KK, Siddiqui MH, Meena R, Verma HN, Kumar S (2013) Cell phone radiation exposure on brain and associated biological systems. Indian J Exp Biol 51(3):187–200PubMedGoogle Scholar
  26. Khadrawy YA, Ahmed NA, Aboul Ezz HS, Radwan NM (2009) Effect of electromagnetic radiation from mobile phone on the levels of cortical amino acid neurotransmitters in adult and young rats. Rom J Biophys 19:295–305Google Scholar
  27. Khorseva NI, Grigor’ev IG, Gorbunova NV (2011) Psychophysiological indicators for children using mobile phones. Communication 2. Results of four-year monitoring. Radiats Biol Radioecol 51(5):617–623PubMedGoogle Scholar
  28. Kumlin T, Iivonen H, Miettinen P, Juvonen A, van Groen T, Puranen L, Pitkäaho R, Juutilainen J, Tanila H (2007) Mobile phone radiation and the developing brain: behavioral and morphological effects in juvenile rats. Radiat Res 168(4):471–479CrossRefPubMedGoogle Scholar
  29. Lai H, Singh NP (1995) Acute low-intensity microwave exposure increases DNA single-strand breaks in rat brain cells. Bioelectromagnetics 16(3):207–210CrossRefPubMedGoogle Scholar
  30. Liu Y, Ma S, Qu RSCLM (2010) Total saponins extracted from Chaihu-jia-longgu-muli-tang, reduces chronic mild stress-induced apoptosis in the hippocampus in mice. Pharm Biol 48(8):840–848CrossRefPubMedGoogle Scholar
  31. Loughran SP, Benz DC, Schmid MR, Murbach M, Kuster N, Achermann P (2013) No increased sensitivity in brain activity of adolescents exposed to mobile phone-like emissions. Clin Neurophysiol 124(7):1303–1308. doi:10.1016/j.clinph.2013.01.010, Epub 2013 Feb 18 CrossRefPubMedGoogle Scholar
  32. Lupien SJ, McEwen BS, Gunnar MR, Heim C (2009) Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 10(6):434–445. doi:10.1038/nrn2639 CrossRefPubMedGoogle Scholar
  33. Maaroufi K, Had-Aissouni L, Melon C, Sakly M, Abdelmelek H, Poucet B, Save E (2014) Spatial learning, monoamines and oxidative stress in rats exposed to 900 MHz electromagnetic field in combination with iron overload. Behav Brain Res 258:80–89. doi:10.1016/j.bbr.2013.10.016 CrossRefPubMedGoogle Scholar
  34. Maskey D, Pradhan J, Aryal B, Lee CM, Choi IY, Park KS, Kim SB, Kim HG, Kim MJ (2010) Chronic 835-MHz radiofrequency exposure to mice hippocampus alters the distribution of calbindin and GFAP immunoreactivity. Brain Res 1346:237–246. doi:10.1016/j.brainres.2010.05.045, Epub 2010 Jun 17 CrossRefPubMedGoogle Scholar
  35. Megha K, Deshmukh PS, Banerjee BD, Tripathi AK, Abegaonkar MP (2012) Microwave radiation induced oxidative stress, cognitive impairment and inflammation in brain of Fischer rats. Indian J Exp Biol 50(12):889–896PubMedGoogle Scholar
  36. Moser MB, Moser EI, Forrest E, Andersen P, Morris RG (1995) Spatial learning with a minislab in the dorsal hippocampus. Proc Natl Acad Sci U S A 92(21):9697–9701PubMedCentralCrossRefPubMedGoogle Scholar
  37. Narayanan SN, Kumar RS, Potu BK, Nayak S, Mailankot M (2009) Spatial memory performance of Wistar rats exposed to mobile phone. Clinics (Sao Paulo) 64(3):231–234CrossRefGoogle Scholar
  38. Narayanan SN, Kumar RS, Potu BK, Nayak S, Bhat PG, Mailankot M (2010) Effect of radio-frequency electromagnetic radiations (RF-EMR) on passive avoidance behaviour and hippocampal morphology in Wistar rats. Ups J Med Sci 115(2):91–96PubMedCentralCrossRefPubMedGoogle Scholar
  39. Narayanan SN, Kumar RS, Paval J, Kedage V, Bhat MS, Nayak S, Bhat PG (2013) Analysis of emotionality and locomotion in radio-frequency electromagnetic radiation exposed rats. Neurol Sci 34(7):1117–1124CrossRefPubMedGoogle Scholar
  40. Narayanan SN, Kumar RS, Kedage V, Nalini K, Nayak S, Bhat PG (2014a) Evaluation of oxidant stress and antioxidant defence in discrete brain regions of rats exposed to 900 MHz radiations. Bratisl Lek Listy 115(5):260–266Google Scholar
  41. Narayanan SN, Raghu J, Gorantla VR, Kumar RS, Nayak S, Bhat PG (2014b) Appraisal of the effect of brain impregnation duration on neuronal staining and morphology in a modified Golgi-cox method. J Neurosci Methods 235:193–207. doi:10.1016/j.jneumeth.2014.07.007, Epub 2014 Jul 23 CrossRefPubMedGoogle Scholar
  42. O’Donnell S, Noseworthy MD, Levine B, Dennis M (2005) Cortical thickness of the frontopolar area in typically developing children and adolescents. Neuroimage 24:948–954CrossRefPubMedGoogle Scholar
  43. Odaci E, Bas O, Kaplan S (2008) Effects of prenatal exposure to a 900 MHz electromagnetic field on the dentate gyrus of rats: a stereological and histopathological study. Brain Res 1238:224–229CrossRefPubMedGoogle Scholar
  44. Olton DS, Papas BC (1979) Spatial memory and hippocampal function. Neuropsychologia 17(6):669–682CrossRefPubMedGoogle Scholar
  45. Partsvania B, Sulaberidze T, Shoshiashvili L (2013) Effect of high SARs produced by cell phone like radiofrequency fields on mollusk single neuron. Electromagn Biol Med 32(1):48–58. doi:10.3109/15368378.2012.701190, Epub 2012 Oct 9 CrossRefPubMedGoogle Scholar
  46. Prichard CT, Alloway KD (1998) Medical neuroscience, 1st edn. Fence Creek Publishing, LLC, Madison, pp 377–383Google Scholar
  47. Ramkumar K, Srikumar BN, Shankaranarayana Rao BS, Raju TR (2008) Self-stimulation rewarding experience restores stress-induced CA3 dendritic atrophy, spatial memory deficits and alterations in the levels of neurotransmitters in the hippocampus. Neurochem Res 33(9):1651–1662CrossRefPubMedGoogle Scholar
  48. Rudi DH, Peter PD (2001) Applications of Morris water maze in the study of learning and memory. Brain Res Rev 36:60–90CrossRefGoogle Scholar
  49. Ruth RE, Collier TJ, Routtenberg A (1982) Topography between the entorhinal cortex and the dentate septotemporal axis in rats: I. Medial and intermediate entorhinal projecting cells. J Comp Neurol 209(1):69–78CrossRefPubMedGoogle Scholar
  50. Saikhedkar N, Bhatnagar M, Jain A, Sukhwal P, Sharma C, Jaiswal N (2014) Effects of mobile phone radiation (900 MHz radiofrequency) on structure and functions of rat brain. Neurol Res 1743132814Y0000000392. [Epub ahead of print]Google Scholar
  51. Sapolsky RM (2000) The possibility of neurotoxicity in the hippocampus in major depression: a primer on neuron death. Biol Psychiatry 48(8):755–765CrossRefPubMedGoogle Scholar
  52. Sauter C, Dorn H, Bahr A, Hansen ML, Peter A, Bajbouj M, Danker-Hopfe H (2011) Effects of exposure to electromagnetic fields emitted by GSM 900 and WCDMA mobile phones on cognitive function in young male subjects. Bioelectromagnetics 32(3):179–190. doi:10.1002/bem.20623, Epub 2010 Oct 28 CrossRefPubMedGoogle Scholar
  53. Schloesser RJ, Jimenez DV, Hardy NF, Paredes D, Catlow BJ, Manji HK, McKay RD, Martinowich K (2014) Atrophy of pyramidal neurons and increased stress-induced glutamate levels in CA3 following chronic suppression of adult neurogenesis. Brain Struct Funct 219(3):1139–1148. doi:10.1007/s00429-013-0532-8, Epub 2013 Mar 13 PubMedCentralCrossRefPubMedGoogle Scholar
  54. Scoville WB, Milner B (1957) Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 20:11–21PubMedCentralCrossRefPubMedGoogle Scholar
  55. Setlow B, McGaugh JL (2000) D2 Dopamine receptor blockade immediately post-training enhances retention in hidden and visible platform versions of the water maze. Learn Mem 7(3):187–191CrossRefPubMedGoogle Scholar
  56. Shankaranarayana Rao BS, Govindaiah, Laxmi TR, Meti BL, Raju TR (2001) Subicular lesions cause dendritic atrophy in CA1 and CA3 pyramidal neurons of the rat hippocampus. Neuroscience 102(2):319–327CrossRefPubMedGoogle Scholar
  57. Sholl DA (1953) Dendritic organization in the neurons of the visual and motor cortices of the cat. J Anat 87(4):387–406PubMedCentralPubMedGoogle Scholar
  58. Sunanda, Shankaranarayana Rao BS, Raju TR (2000) Chronic restraint stress impairs acquisition and retention of spatial memory task in rats. Curr Sci 799(11):1581–1584Google Scholar
  59. Titus AD, Shankaranarayana Rao BS, Harsha HN, Ramkumar K, Srikumar BN, Singh SB, Chattarji S, Raju TR (2007) Hypobaric hypoxia-induced dendritic atrophy of hippocampal neurons is associated with cognitive impairment in adult rats. Neuroscience 145(1):265–278CrossRefPubMedGoogle Scholar
  60. Tsamis IK, Mytilinaios GD, Njau NS, Fotiou FD, Glaftsi S, Costa V, Baloyannis JS (2010) Properties of CA3 dendritic excrescences in Alzheimer’s disease. Curr Alzheimer Res 7(1):84–90CrossRefPubMedGoogle Scholar
  61. Valentini E, Ferrara M, Presaghi F, De Gennaro L, Curcio G (2010) Systematic review and meta-analysis of psychomotor effects of mobile phone electromagnetic fields. Occup Environ Med 67(10):708–716. doi:10.1136/oem.2009.047027 CrossRefPubMedGoogle Scholar
  62. Vazquez DM, Akil H (1993) Pituitary-adrenal response to ether vapor in the weanling animal: characterization of the inhibitory effect of glucocorticoids on adrenocorticotropin secretion. Pediatr Res 34:646–653CrossRefPubMedGoogle Scholar
  63. Witter MP, Groenewegen HJ, Lopes da Silva FH, Lohman AH (1989) Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog Neurobiol 33(3):161–253CrossRefPubMedGoogle Scholar
  64. World Health Organization (2011) Electromagnetic fi elds and public health: mobile phones, Fact sheet No193. http://www.who.int/mediacentre/factsheets/fs193/en/
  65. Yu-Hong Z, Yong Z, Tong-Jun Z, Ying-Rong H, Hui L (2007) Mechanism of permeation in calcium channels activation by applied magnetic fields. Conf Proc IEEE Eng Med Biol Soc 2007:1391–1393PubMedGoogle Scholar
  66. Zhao TY, Zou SP, Knapp PE (2007) Exposure to cell phone radiation up-regulates apoptosis genes in primary cultures of neurons and astrocytes. Neurosci Lett 412(1):34–38PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Sareesh Naduvil Narayanan
    • 1
  • Raju Suresh Kumar
    • 1
    • 5
  • Kalesh M. Karun
    • 2
  • Satheesha B. Nayak
    • 3
  • P. Gopalakrishna Bhat
    • 4
  1. 1.Department of Physiology, Melaka Manipal Medical College (Manipal Campus)Manipal UniversityManipalIndia
  2. 2.Department of StatisticsManipal UniversityManipalIndia
  3. 3.Department of Anatomy, Melaka Manipal Medical College (Manipal Campus)Manipal UniversityManipalIndia
  4. 4.Division of Biotechnology, School of Life SciencesManipal UniversityManipalIndia
  5. 5.College of Science and Health Professions – JeddahKing Saud Bin Abdulaziz University for Health Sciences, National Guard Health AffairsJeddahKingdom of Saudi Arabia

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